Dual tasking impairments are associated with striatal pathology in Huntington's disease.

Johnny Lo,Timothy J Rankin,Kirk Feindel,Danielle M Bartlett,Travis M Cruickshank,Alvaro Reyes,Timothy S Pulverenti,Mel R Ziman,Pauline Zaenker,Govinda Poudel,Grant Rowe,Nellie Georgiou‐Karistianis

doi:10.1002/acn3.51142

Abstract

BackgroundRecent findings suggest that individuals with Huntington’s disease (HD) have an impaired capacity to execute cognitive and motor tasks simultaneously, or dual task, which gradually worsens as the disease advances. The onset and neuropathological changes mediating impairments in dual tasking in individuals with HD are unclear. The reliability of dual tasking assessments for individuals with HD is also unclear.ObjectivesTo evaluate differences in dual tasking performance between individuals with HD (presymptomatic and prodromal) and matched controls, to investigate associations between striatal volume and dual tasking performance, and to determine the reliability of dual tasking assessments.MethodsTwenty individuals with HD (10 presymptomatic and 10 prodromal) and 20 healthy controls were recruited for the study. Individuals undertook four single and dual task assessments, comprising motor (postural stability or force steadiness) and cognitive (simple or complex mental arithmetic) components, with single and dual tasks performed three times each. Participants also undertook a magnetic resonance imaging assessment.ResultsCompared to healthy controls, individuals with presymptomatic and prodromal HD displayed significant deficits in dual tasking, particularly cognitive task performance when concurrently undertaking motor tasks (P < 0.05). The observed deficits in dual tasking were associated with reduced volume in caudate and putamen structures (P < 0.05),however, not with clinical measures of disease burden. An analysis of the reliability of dual tasking assessments revealed moderate to high test–retest reliability [ICC: 0.61‐0.99] for individuals with presymptomatic and prodromal HD and healthy controls.ConclusionsIndividuals with presymptomatic and prodromal HD have significant deficits in dual tasking that are associated with striatal degeneration. Findings also indicate that dual tasking assessments are reliable in individuals presymptomatic and prodromal HD and healthy controls.

Highlights

Existing studies have documented deficits in bimanual tapping, walking while talking and speed accuracy tradeoff tasks in individuals with manifest Huntington’s disease (HD).[3,5,6,7,8,9]. Such deficits worsen with increasing task difficulty and are predictive of cognitive and motor impairments in HD.4,6,10While these findings provide compelling evidence that dual tasking impairments are a prominent feature of manifest HD, whether these deficits exist during the premanifest stages and whether progressive striatal degeneration underpins these deficits remains unclear
Nieuwhof et al (2017) documented significant associations between pathological alterations in striatal activation and dual tasking deficits in individuals with Parkinson’s disease (PD). These results suggest that striatal degeneration, at least in part, underpins deficits in dual tasking in individuals with HD and perhaps individuals with striatal pathology in general
For the first time, that dual tasking impairments are present in individuals with pre-HD proHD and are associated with striatal degeneration

Summary

Introduction

The simultaneous execution of cognitive and motor tasks (i.e., dual tasking) is essential for activities of daily living, including driving and maintaining balance.1,2Recent evidence suggests that individuals with Huntington’s disease (HD) have greater difficulty executing dual tasks than healthy controls, which adversely impacts on their functional independence and quality of life.[3,4]Existing studies have documented deficits in bimanual tapping, walking while talking and speed accuracy tradeoff tasks in individuals with manifest HD.[3,5,6,7,8,9] Such deficits worsen with increasing task difficulty and are predictive of cognitive and motor impairments in HD.4,6,10While these findings provide compelling evidence that dual tasking impairments are a prominent feature of manifest HD, whether these deficits exist during the premanifest stages and whether progressive striatal degeneration underpins these deficits remains unclear.The striatum, which shows early and strikingly selective degeneration in HD,[11,12,13] has been suggested to be fundamentally involved in dual tasking.[14]. During this period of the disease, participants are characterized as having presymptomatic HD(pre-HD; little to no clinical signs) orprodromal HD (pro-HD; subtle, but unequivocal signs to warrant formal diagnosis of the disease). Objectives: To evaluate differences in dual tasking performance between individuals with HD (presymptomatic and prodromal) and matched controls, to investigate associations between striatal volume and dual tasking performance, and to determine the reliability of dual tasking assessments. Results: Compared to healthy controls, individuals with presymptomatic and prodromal HD displayed significant deficits in dual tasking, cognitive task performance when concurrently undertaking motor tasks (P < 0.05). Findings indicate that dual tasking assessments are reliable in individuals presymptomatic and prodromal HD and healthy controls

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